Incompatibility and Competitive Exclusion of Genomic Segments between Sibling Species

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The extent and nature of genetic incompatibilities between incipient races and sibling species is of fundamental importance to our view of speciation. However, with the exception of hybrid inviability and sterility factors, little is known about the extent of other, more subtle genetic incompatibilities between incipient species. Here we experimentally demonstrate the prevalence of such genetic incompatibilities between two young allopatric sibling species, Drosophila simulans and D. sechellia. Our experiments took advantage of 12 introgression lines that carried random introgressed D. sechellia segments in different parts of the D. simulans genome. First, we found that these introgression lines did not show any measurable sterility or inviability effects. To study if these sechellia introgressions in a simulans background contained other fitness consequences, we competed and genetically tracked the marked alleles within each introgression against the wild-type alleles for 20 generations. Strikingly, all marked D. sechellia introgression alleles rapidly decreased in frequency in only 6 to 7 generations. We then developed computer simulations to model our competition results. These simulations indicated that selection against D. sechellia introgression alleles was high (average s = 0.43) and that the marker alleles and the incompatible alleles did not separate in 78% of the introgressions. The latter result likely implies that most introgressions contain multiple genetic incompatibilities. Thus, this study reveals that, even at early stages of speciation, many parts of the genome diverge to a point where introducing foreign elements has detrimental fitness consequences, but which cannot be seen using standard sterility and inviability assays.

Vyšlo v časopise: Incompatibility and Competitive Exclusion of Genomic Segments between Sibling Species. PLoS Genet 8(6): e32767. doi:10.1371/journal.pgen.1002795
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002795

Souhrn

Zdroje

1. DobzhanskyT 1937 Genetics and the origin of species New York Columbia University Press 364

2. MayrE 1959 Where are we? Cold Spring Harbor Symp Quant Biol 24 1 14

3. MayrE 1963 Animal species and evolution Cambridge Belknap Press 811

4. MayrE 1954 Change of genetic environment and evolution. HuxleyJHardyACFordEB Evolution as a process London Allen & Unwin 157 180

5. CoyneJOrrA 2004 Speciation Sunderland Sinauer Associates, Inc 545

6. WuCI 2001 The genic view of the process of speciation. J Evol Biol 14 851 865

7. BartonNH 2008 The effect of a barrier to gene flow on patterns of geographic variation. Genet Res 90 139 149

8. ViaS 2009 Natural selection in action during speciation. Proc Natl Acad Sci USA 106 9939 9946

9. TurnerTLHahnMWNuzhdinSV 2005 Genomic islands of speciation in Anopheles gambiae. PLoS Biol 3 e285 doi:10.1371/journal.pbio.0030285

10. HarrB 2006 Genomic islands of differentiation between house mouse subspecies. Genome Res 16 730 737

11. YatabeYKaneNCScotti-SaintagneCRiesebergLH 2007 Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 175 1883 1893

12. NosilPFunkDJOrtiz-BarrientosD 2009 Divergent selection and heterogeneous genomic divergence. Mol Ecol 18 375 402

13. ButlinRK 2010 Population genomics and speciation. Genetica 138 409 418

14. FederJLNosilP 2010 The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution 64 1729 1747

15. MichelAPSimSPowellTHTaylorMSNosilP 2010 Widespread genomic divergence during sympatric speciation. Proc Natl Acad Sci USA 107 9724 9729

16. LawniczakMKNEmrichSJHollowayAKRegierAPOlsonM 2010 Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 330 512 514

17. YukilevichRTurnerTLAokiFNuzhdinSVTrueJR 2010 Patterns and processes of genome-wide divergence between North American and African Drosophila melanogaster. Genetics 186 219 239

18. WuCIPalopoliMF 1994 Genetics of postmating reproductive isolation in animals. Annu Rev Genet 28 283 308

19. TrueJRWeirBSLaurieCC 1996 A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics 142 819 837

20. NaveiraHMasideX 1998 The genetics of hybrid male sterility in Drosophila. HowardDJBerlocherSH Endless forms: species and speciation Oxford Oxford University Press 330 338

21. TaoYChenSHartlDLLaurieCC 2003 Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. I. Differential accumulation of hybrid male sterility effects on the X and autosomes. Genetics 164 1383 1397

22. PresgravesDC 2003 A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics 163 955 972

23. MaslyJPPresgravesDC 2007 High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biol 5 e243 doi:10.1371/journal.pbio.0050243

24. TingCTTsaurSCWuMLWuCI 1998 A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282 1501 1504

25. WittbrodtJAdamDMalitschekBMauelerWRaulfF 1989 Novel putative receptor tyrosine kinase encoded by the melanoma-inducing Tu locus in Xiphophorus. Nature 341 415 421

26. BarbashDASiinoDFTaroneAMRooteJ 2003 A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci USA 100 5302 5307

27. BarbashDAAwadallaPTaroneAM 2004 Functional divergence caused by ancient positive selection of a Drosophila hybrid incompatibility locus. PLoS Biol 2 e142 doi:10.1371/journal.pbio.0020142

28. PresgravesDCBalagopalanLAbmayrSMOrrHA 2003 Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423 715 719

29. BrideauNJFloresHAWangJMaheshwariSWangX 2006 Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314 1292 1295

30. MaslyJPJonesCDNoorMALockeJOrrHA 2006 Gene transposition as a cause of hybrid sterility in Drosophila. Science 313 1448 1450

31. PhadnisNOrrHA 2009 A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323 376 379

32. JohnsonNA 2010 Hybrid incompatibility genes: remnants of a genomic battlefield? Trends Genet 26 317 325

33. BartonNHGaleKS 1993 Genetic analysis of hybrid zones. HarrisonRG Hybrid zones and the evolutionary process Oxford Oxford University Press 13 45

34. MercerKLWyseDLShawRG 2006 Effects of competition on fitness of wild and crop-wild hybrid sunflower from a diversity of wild populations and crop lines. Evolution 60 2044 2055

35. BartonNHHewittGM 1981 Hybrid zones and speciation. AtchleyWRWoodruffD Evolution and Speciation Cambridge Cambridge University Press 109 145

36. RiesebergLHWhittonJGardnerK 1999 Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152 713 727

37. McDermottSRKlimanRM 2008 Estimation of isolation times of the island species in the Drosophila simulans complex from multilocus DNA sequence data. PLoS ONE 3 e2442 doi:10.1371/journal.pone.0002442

38. LachaiseDDavidJRLemeunierFTsacasLAshburnerM 1986 The reproductive relationships of Drosophila sechellia with D. mauritiana, D. simulans, and D. melanogaster from the Afrotropical region. Evolution 40 262 271

39. LachaiseDCariouMLDavidJRLemeunierFTsacasL 1988 Historical biogeography of the Drosophila melanogaster species subgroup. Evol Biol 22 159 225

40. LachaiseDSilvainJF 2004 How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle. Genetica 120 17 39

41. HaldaneJBS 1924 A mathematical theory of natural and artificial selection, Part I. Trans Camb Philos Soc 23 19 41

42. SharpPM 1984 The effect of Inbreeding on competitive male-mating ability in Drosophila melanogaster. Genetics 106 601 612

43. SpencerLJSnowAA 2001 Fecundity of transgenic wild-crop hybrids of Cucurbita pepo (Cucurbitaceae): implications for crop-to-wild gene flow. Heredity 86 694 702

44. StewartCNJrHalfhillMDWarwickSI 2003 Transgene introgression from genetically modified crops to their wild relatives. Nat Rev Gen 4 806 817

45. SongZPLuBRWangBChenJK 2004 Fitness estimation through performance comparison of F1 hybrids with their parental species Oryza rufipogon and O. sativa. Ann Bot 93 311 316

46. WrightS 1932 The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proc Sixth Inter Congr Genet 1 356 366

47. GavriletsS 2004 Fitness landscapes and the origin of species Princeton Princeton University Press 432

48. CarterAJHermissonJHansenTF 2005 The role of epistatic gene interactions in the response to selection and the evolution of evolvability. Theor Popul Biol 68 179 196

49. OrrHA 2006 The population genetics of adaptation on correlated fitness landscapes: the block model. Evolution 60 1113 1124

50. YukilevichRLachanceJAokiFTrueJR 2008 Long-term adaptation of epistatic genetic networks. Evolution 62 2215 2235

51. GavriletsS 2000 Waiting time to parapatric speciation. Proc Biol Sci 267 2483 2492

52. WadeMJ 2002 A gene's view of epistasis, selection and speciation. J Evol Biol 15 337 346

53. MacdonaldSJGoldsteinDB 1999 A quantitative genetic analysis of male sexual traits distinguishing the sibling species Drosophila simulans and D. sechellia. Genetics 153 1683 1699

54. ColsonIMacDonaldSJGoldsteinDB 1999 Microsatellite markers for interspecific mapping of Drosophila simulans and D. sechellia. Mol Ecol 8 1951 1955

55. WuCIHollocherHBegunDJAquadroCFXuY 1995 Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation. Proc Natl Acad Sci USA 92 2519 2523

56. CasaresPCarracedoMCRioBDPiñeiroRGarcía-FlórezL 1998 Disentangling the effects of mating propensity and mating choice in Drosophila. Evolution 52 126 133